Pommery et al. BMC Ecol Evo (2021) 21:136 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01835-4

RESEARCH Open Access Dentition and feeding in Placodontia: tooth replacement in Henodus chelyops Yannick Pommery1,2,3, Torsten M. Scheyer4 , James M. Neenan5 , Tobias Reich4, Vincent Fernandez6,7 , Dennis F. A. E. Voeten6,8,9 , Adrian S. Losko10 and Ingmar Werneburg1,2*

Abstract Background: Placodontia is a Triassic sauropterygian reptile group characterized by fat and enlarged crushing teeth adapted to a durophagous diet. The enigmatic placodont Henodus chelyops has numerous autapomorphic character states, including extreme tooth count reduction to only a single pair of palatine and dentary crushing teeth. This ren- ders the species unusual among placodonts and challenges identifcation of its phylogenetic position. Results: The skulls of two Henodus chelyops specimens were visualized with synchrotron tomography to investigate the complete anatomy of their functional and replacement crushing dentition in 3D. All teeth of both specimens were segmented, measured, and statistically compared to reveal that H. chelyops teeth are much smaller than the posterior palatine teeth of other cyamodontoid placodonts with the exception of Parahenodus atancensis from the Iberian Peninsula. The replacement teeth of this species are quite similar in size and morphology to the functional teeth. Conclusion: As other placodonts, Henodus chelyops exhibits vertical tooth replacement. This suggests that verti- cal tooth replacement arose relatively early in placodont phylogeny. Analysis of dental morphology in H. chelyops revealed a concave shape of the occlusal surface and the notable absence of a central cusp. This dental morphology could have reduced dental wear and protected against failure. Hence, the concave teeth of H. chelyops appear to be adapted to process small invertebrate items, such as branchiopod crustaceans. Small gastropods were encountered in the matrix close to both studied skulls. Keywords: Synchrotron tomographic scans, Functional morphology, Jaw mechanism, Ontogeny, Evolution, Triassic

Background were found in Europe [4–9], in the Middle East [10], and Te extinct Sauropterygia is one of the most diversifed in Asia [11–16]. Tese remains are known from "Oberer clades of Mesozoic marine reptiles that encompasses Buntsandstein", Anisian [17, 18] to Rhaetian [19] times. pachypleurosaurs, nothosaurs, pistosaurs, plesiosaurs, Placodonts died out in or just before the Triassic-Jurassic and placodonts [1]. Placodonts are among the frst sau- extinction event (~ 201.3 Ma) without any descendants ropterygians to appear in the fossil record [1, 2]. Te frst [20]. Teir relative rarity and uncertainty regarding the material of Placodontia was described by Münster [3] exact age of several placodont-bearing deposits renders from the Bavarian Muschelkalk. Since then, its remains reconstruction of the stratigraphical and geographical distribution of Placodontia particularly challenging [21]. Nevertheless, the geological context indicates that pla- *Correspondence: [email protected] codonts inhabited shallow water near the northeastern 1 Senckenberg Centre for Human Evolution and Palaeoenvironment (HEP) an der Eberhard-Karls-Universität Tübingen, Sigwartstraße 10, and -western Tethys coastal margins [13, 21–23]. Tis 72076 Tübingen, Germany restricted geographical range may refect their specifc Full list of author information is available at the end of the article diet consisting of hard-shelled prey [24]. Placodonts

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feature a rather rigid body, a single pair of temporal Psephoderma, Psephochelys, and Macroplacus represent fenestrae, and a dental architecture (crushing teeth) Placochelyidae. Henodontidae consists of Henodus with adapted to a durophagous diet [21, 25]. the single species H. chelyops and the recently described species Parahenodus atancensis [8, 16, 38]. Parahenodus Placodontia dentition atancensis is represented only by a single partial cranium. Skull reconstructions across placodont diversity permits H. chelyops shares several characters with other cyamo- interspecifc comparison [24]. Besides cranial topology, dontoid placodonts, such as a short and broad carapace, the identifcation of placodont taxa also strongly relies on cranial tubercles, reducted dentition, and the separa- dental morphology (e.g., [26–29]). Te dentition of placo- tion of the nasals with Placochelyidae [24]. H. chelyops donts has been studied intensively towards understand- occurred rather late in stratigraphical deposits, which ing the variability of dental morphology and inferred may imply that this taxon is deeply nested in placodont feeding behavior across this group [2, 24, 27–33]. Tooth phylogeny but could also refect a preservation bias [36]. location, anatomy, and replacement pattern aids in phy- logenetic inferences (e.g., [29, 33]). Te dentition and the upper jaw of all major placodont groups are known for Henodus chelyops remains their good preservation and can be compared with each Henodus chelyops was frst assigned to Placodontia by v. other. Teeth are supported by the premaxilla, maxilla, and Huene in 1936 [18]. All H. chelyops remains have been palatine in the cranium, and the dentary in the mandible. discovered as well-preserved elements at one locality Paraplacodus and Placodus have long and procumbent exposing the “Oberer Gipskeuper” of the village of Lust- teeth, similar to Palatodonta bleekeri, on the premaxil- nau near Tübingen (Baden-Württemberg, Germany). lary and the anterior part of the dentary [24, 29, 34]. In Tese deposits date from the Carnian, and are com- Placodus, these chisel-shaped teeth have a deep root and posed of grey shales with thin silt laminae [18, 39, 40]. a more horizontally oriented alveolus [32]. Cyamodus Tese shales have been interpreted as being “ephemeral and Protenodontosaurus are the rare representatives of lacustrine to restricted shallow-marine” deposits [40]. H. Cyamodontoidea to bear premaxillary teeth [29, 35]. Te chelyops represents the only known placodont to have maxillary and palatine teeth, in contrast, are adapted for inhabited a brackish lagoonal environment. Several auta- crushing and feature short roots, shallow alveoli, and an pomorphic character states were described for this spe- ankylosed thecodont tooth implantation [24, 32]. Placo- cies, such as its roughly rectangular and fat skull, its chelyid placodonts have fewer teeth than other placodont wide rostrum, and its very deep and massive lower jaw [8, groups. In Placochelys and Psephoderma, as in H. chely- 18, 24, 26, 31, 36, 38, 41, 42] (Fig. 1). ops, premaxillary teeth (and antagonistic dentary coun- terparts) are absent in the narrow rostrum [24]. Henodus chelyops dentition Placodont phylogeny Te dentition of H. chelyops is extremely reduced [18, Since the end of the twentieth century, the phylogeny 24, 26, 27, 31, 41]. Te dentition of H. chelyops lacks pre- of Placodontia has been frequently addressed (e.g., [1, maxillary and maxillary teeth and involves a single pair 2, 5, 13–17, 21, 25, 34, 36]). Placodontiformes repre- of crushing teeth located across the posterior part of the sents the sister-group to all remaining sauropterygians, palatines that occludes with a corresponding pair of teeth the Eosauropterygia [37]. Placodontiformes is the group across the dentaries. Te dental antagonists on the lower that includes the non-placodont Palatodonta bleekeri as jaw are situated medially to the small coronoid processes sister taxon to Placodontia [2]. Paraplacodus is consid- on the dentary [18]. Te pair of teeth on the upper jaw is ered as sister of all remaining placodonts regarding its homologous to the posterior-most palatine teeth of other relatively plesiomorphic dentition and complete lack of placodonts [18, 31]. osteoderms in the postcranial skeleton [24, 34, 36]. Mul- Te complex of autapomorphic character states for H. tiple phylogenetic analyses converged on distinguishing chelyops has confounded inference of its phylogenetic the monophyletic clade Cyamodontoidea from the non- position within Placodontia for decades [1, 36]. Te atyp- armored placodonts Paraplacodus and Placodus [1, 5, ical ‘dentition’ of H. chelyops comprises a unique combi- 16, 34]. Cyamodontoidea is subdivided into the two taxa nation of three structures—a cutting edge with denticles, Cyamodontida and Placochelyida [1, 16]. Cyamodontida baleen-like grooves, and crushing palatine teeth—that is known through Cyamodus and Sinocyamodus [16]. inspired numerous hypotheses on its feeding behavior Placochelyida is composed of the early Protenodontosau- that range from flter feeding and suction feeding to her- rus italicus and the two clades Placochelyidae and Heno- bivory. Durophagy, which is ubiquitous across other pla- dontidae [16]. Te genera Placochelys, Glyphoderma, codonts, likely played only a moderate role in this taxon. Pommery et al. BMC Ecol Evo (2021) 21:136 Page 3 of 19

Fig. 1 Macroscopic picture of the skull of Henodus chelyops specimen GPIT-PV-30003 in ventral (A), dextral (B), dorsal (C) and frontal (D) views. The mandible is still articulated with the cranium

Challenges and aims of the study 33, 46]. Tis dental replacement mode does not seem to Te recent development of state-of-the-art tomo- have appeared independently among diferent placodont graphic imaging techniques allows for the investigation groups. Tooth replacement has not yet been determined of internal anatomical features such as the braincase, for Henodontidae. Studying the replacement pattern of endocranium, and even replacement teeth [2, 43–45]. the reduced palatine crushing teeth in H. chelyops will Re-examination of well-studied fossils with these non- therefore not only provide insight into the ecomorphol- destructive methods can ofer 3D insight in previously ogy and diet of this enigmatic taxon, but will also aid in inaccessible morphological features. Te dentition of understanding the evolutionary diversity of dental mor- H. chelyops is rarely visible, as it is typically covered by phology and replacement strategies across Placodontia. sediment, or obscured by the cranium and mandibular elements. Recently generated synchrotron tomographic Results scans of the skulls of several H. chelyops individuals are Tooth position and morphology now available in the Paleontological Collection of the PPC SRµCT data of the skulls of specimens GPIT- University of Tübingen and in the Paleobiology Database PV-30003 and GPIT-PV-30007 uncovered morphological of the ESRF. Tese data expose internal structures of H. details of H. chelyops that are not visible in external view. chelyops crania and mandibles and permit the frst exten- Tus, it was possible to visualize the internal structure of sive study of crushing tooth replacement in H. chelyops. the skulls but also the functional and replacement crush- Te dentition of this taxon has not been examined since ing teeth. However, cracks, likely flled with minerals rich Reif and Stein [31]. in metallic elements, are present in several parts of the Tis study aims to describe the anatomy of the crush- skulls making it difcult to observe the internal struc- ing teeth in H. chelyops with particular attention to the tures. Indeed, they prevent a precise distinction of bone occlusal surface morphology in H. chelyops, and also sets structures. A few teeth are cracked due to poor preserva- out to explain the tooth replacement pattern of this spe- tion. All crushing teeth are situated on the posterior part cies relative to those in other placodonts. Based on the of the palatine and of the dentary. Both specimens carry above observations, we hypothesize that vertical tooth functional and replacement teeth on the upper and lower replacement is a synapomorphy for Placodontia [30, 32, Pommery et al. BMC Ecol Evo (2021) 21:136 Page 4 of 19

jaws (Fig. 2). A single functional crushing tooth is located lower jaw (Fig. 2). Te functional crushing tooth of the on each palatine and dentary. right palatine in specimen GPIT-PV-30003 seems to Specimens GPIT-PV-30003 and GPIT-PV-30007 both have moved while burying. It is shifted to the left side have a total of four functional teeth, each of which has and seems not to be attached to the palatine. a corresponding single replacement tooth so that there Te crushing teeth in H. chelyops are larger in only is a single generation of tooth replacement in the anteroposterior axis than in the dextrosinistral these specimens visible (Fig. 2). Teeth are moderately axis. Tey generally have an ovoid shape (Fig. 3). Te tilted backward. Te tooth replacement is vertical. Te replacement teeth have a similar shape to the func- replacement tooth is situated in an alveolus deep to the tional ones. Tey are not really fattened as previously functional tooth. Te orientation of the replacement mentioned [31] but curved with the occlusal surface tooth is basically parallel to the functional tooth. Te being slightly concave. Some slight morphological dif- distance between the functional tooth and the associ- ferences appear between replacement and functional ated replacement tooth does not appear to be equiva- teeth (Fig. 3). Mostly, the thick enamel layer is more lent between all the teeth of a single specimen. Te marked and larger (around 1 mm) on the replacement disparity of the distance between the replacement and teeth than on the functional ones. Te progressive wear the functional tooth observed in this study could illus- of the functional teeth can explain why the thin layer of trate the migration of the replacement tooth and dif- enamel is less observable. Te replacement teeth have ferent stages in the replacement process in H. chelyops. a little root (Fig. 3) that is less visible for the functional Otherwise, this disparity could be the result of a tapho- teeth likely due to the ankylosis of the teeth to the alve- nomic process. Te position of the functional teeth of olar bone. the upper jaw matches with the functional teeth of the

Fig. 2 3D model in dextral (A) and antero-dorsal (B) views of specimen GPIT-PV-30003 exposing the position of the replacement and functional teeth on both upper (teeth in blue) and lower (teeth in green) jaws in Henodus chelyops. The replacement teeth are represented with light colors. 75% of transparency was applied to the skull. 2D saggitallice (C) and illustration (D) allow to obtain more detailed visualization of the position of the teeth Pommery et al. BMC Ecol Evo (2021) 21:136 Page 5 of 19

Te bivariate diagrams of the length, width, and height of replacement and functional teeth are given in Fig. 4. Te values were sorted according to tooth length for each specimen. Te size values in specimen GPIT-PV-30007 are generally higher than in specimen GPIT-PV-30003. For example, the tooth width in speci- men GPIT-PV-30003 does not exceed 8 mm whereas, in specimen GPIT-PV-30007, it is between approximatively 8 and 10 mm. Te smallest replacement and functional teeth in specimen GPIT-PV-30007 have a similar length to those of specimen GPIT-PV-30003. For each speci- men, the longer the teeth are, the wider they are, but this is not the case for their height (Fig. 4). Te size values for specimen GPIT-PV-30003 are rather clustered when compared to specimen GPIT-PV-30007. Te same results were obtained by normalizing the tooth size values with skull length. It was chosen not to mix the values of both specimens for the rest of this study in view of these observations. Te boxplots also reveal the size variation of the func- tional and the replacement teeth in specimens GPIT- PV-30003 and GPIT-PV-30007, and diferences can be Fig. 3 Comparison of the morphology of palatine replacement observed for the tooth length, width, and height (Fig. 4). (A, light blue) and functional (B, blue) teeth in Henodus chelyops (specimen GPIT-PV-30007) in occlusal (left) and lingual (right) views. Te boxplots of the tooth width and height indicate that The black arrow shows the short root on the replacement tooth the size ranges of the replacement teeth of both speci- mens do not overlap, as shown in the bivariate diagrams. Te replacement teeth in specimen GPIT-PV-30007 are wider and higher than in specimen GPIT-PV-30003. Size measurements It is also the case for the functional teeth. However, the Te measurements of the length, the width, and the length range of the functional teeth matches with the height of each tooth were repeated ten times (see length range of the replacement teeth in each specimen. Table 1). Te means, the standard deviations, and the Te length ranges of the teeth of both specimens overlap. standard and relative errors have also been added. For Te medians of the tooth width and the height in speci- both specimens, the replacement teeth are on aver- men GPIT-PV-30003 are always lower than in specimen GPIT-PV-30007. Moreover, the median of the length of age 13.23 ± 1.23 mm long, 8.15 ± 0.59 mm wide, and the replacement teeth is higher than the functional teeth 2.55 ± 0.19 mm in height (Table 2). Te functional teeth in both specimens. are 12.23 ± 1.45 mm long, 7.65 ± 1.05 mm wide, and The resulting p-values from the Mann–Whit- 2.69 ± 0.17 mm in height (Table 2). In light of these means, the replacement teeth tend to be longer and ney U test to compare the length, the width, and the wider than the functional teeth in these specimens. How- height between the replacement and functional teeth ever, they are smaller in height, which could indicate for each specimen are as follows: in specimen GPIT- that the replacement teeth are not fully developed. Te PV-30003, the p-value of the tooth length is 0.05714, relative errors of the tooth length range from 0.052 to while the p-value is 0.0294 for the tooth width, and 0.2 0.405%. Te minimum of the relative errors of the tooth for the tooth height. In specimen GPIT-PV-30007, the width is 0.124% and the maximum is 0.672%. Te rela- p-value of the length is 1, 0.6857 for the tooth width, tive errors of the tooth height are between 0.269% and and 0.4678 for the tooth height. The majority of the 1.235%. It should be noted that the measurements of the p-values are greater than 0.05, leading to the accept- tooth height are more dispersed than the measurements ance of the null hypothesis that there is no significant of the tooth length and width. Tese diferences could be size difference between replacement and functional the efect of the positioning of the 3D models. It is nec- teeth in H. chelyops. These high values are partly the essary to remain prudent with these results. Indeed, the result of the low number of tooth samples. However, dental wear and the preservation could create a bias on the widths of the replacement and functional teeth in the measured size of the segmented teeth. specimen GPIT-PV-30003 are significantly different Pommery et al. BMC Ecol Evo (2021) 21:136 Page 6 of 19 Height 3_4 Height 3_8 Height 7_4 Height 2.58 2.6 2.58 2.46 2.58 2.62 2.44 2.5 2.72 2.44 2.56 2.44 2.44 2.54 2.46 2.58 2.58 2.68 2.52 2.68 2.68 2.64 2.38 2.54 2.498 2.59 0.061 0.091 0.019 0.029 0.739 1.148 Width 3_4 Width 3_8 Width 7_4 Width 7.3 6.26 9.8 7.16 6.34 9.68 7.46 6.3 9.66 7.46 6.14 9.6 7.4 6.28 7.38 6.5 7.62 6.3 7.32 6.2 7.16 6.34 7.14 6.14 7.34 6.28 0.107 0.156 0.034 0.049 0.537 0.672 0.126 0.125 0.04 0.04 0.376 0.348 Length 3_4 Length 3_8 Length 7_4 Length 11.54 10.58 16.34 11.48 10.5 16.3 11.46 10.6 16.38 11.5 10.46 16.3 11.4 10.58 11.3 10.8 11.48 10.8 11.46 10.44 11.14 10.54 11.28 10.52 11.404 10.582 Height 3_3 Height 3_7 Height 7_3 Height 2.46 2.28 2.72 2.36 2.18 2.82 2.38 2.22 2.78 2.36 2.28 2.78 2.42 2.22 2.42 2.38 2.44 2.28 2.42 2.28 2.4 2.32 2.42 2.2 2.408 2.264 0.06 0.033 0.019 0.01 0.841 0.432 Width 3_3 Width 3_7 Width 7_3 Width 5.68 7.32 8.98 5.68 7.18 9.06 5.86 7.4 9.06 5.72 7.42 8.96 5.7 7.24 5.76 7.18 5.68 7.24 5.72 7.46 5.68 7.36 5.52 7.52 5.7 7.332 0.119 0.084 0.038 0.027 0.515 0.468 0.087 0.027 0.223 Length 3_3 Length 3_7 Length 7_3 Length 9.72 12.4 12.64 9.92 12.36 12.5 9.82 12.46 12.72 9.88 12.24 12.54 9.88 12.32 9.82 12.34 9.84 12.2 9.84 12.26 9.8 12.2 10,00 12.36 9.852 12.314 0.075 0.024 0.241 Height 3_2 Height 3_6 Height 7_2 Height 2.36 2.78 2.6 2.28 2.74 2.64 2.36 2.64 2.74 2.24 2.74 2.72 2.36 2.74 2.38 2.52 2.28 2.6 2.34 2.7 2.32 2.6 2.4 2.54 2.332 2.66 0.051 0.092 0.029 0.016 1.098 0.691 Width 3_2 Width 3_6 Width 7_2 Width 6.7 6.86 8.96 6.74 6.86 9.08 6.7 6.7 9.02 6.82 6.88 9.04 6.66 6.64 6.8 6.78 6.64 6.42 6.64 6.72 6.64 6.62 6.66 6.76 6.7 6.724 0.067 0.14 0.044 0.021 0.659 0.315 0.132 0.076 0.024 0.042 0.196 0.405 Length 3_2 Length 3_6 Length 7_2 Length 10.38 12.26 11.34 10.1 12.2 11.56 10.46 12.04 11.3 10.44 12.16 11.58 10.34 12.14 10.2 12.28 10.26 12.12 10.4 12.24 10.44 12.26 10.14 12.18 10.316 12.188 Height 3_1 Height 3_5 Height 7_1 Height 2.42 2.24 2.92 2.32 2.34 2.84 2.34 2.34 2.92 2.48 2.3 2.88 2.34 2.18 2.3 2.24 2.36 2.12 2.28 2.14 2.36 2.12 2.36 2.16 2.356 2.218 0.058 0.087 0.027 0.018 1.235 0.778 Width 3_1 Width 3_5 Width 7_1 Width 7.64 7.64 9.54 7.62 7.9 9.8 7.62 7.78 9.8 7.66 7.62 9.8 7.56 7.84 7.6 7.82 7.62 7.82 7.58 7.62 7.52 7.66 7.54 7.7 7.596 7.74 0.045 0.104 0.033 0.014 0.424 0.187 0.065 0.165 0.052 0.02 0.393 0.158 Length 3_1 Length 3_5 Length 7_1 Length 12.98 12.94 16,00 12.78 13.12 15.98 12.94 13.42 15.78 12.9 13.42 16.02 12.96 13.24 12.96 13.42 12.96 13.4 12.94 13.4 13.02 13.4 12.9 13.4 12.934 13.316 Repeated measurements of the length, the width, and the height of each segmented tooth in specimens GPIT-PV-30003 and GPIT-PV-30007 in specimens GPIT-PV-30003 tooth of the length, width, and height each segmented measurements Repeated 1 Table Measurement Measurement Measurement 1 1 1 2 2 2 3 3 3 4 4 4 5 5 6 6 7 7 8 8 9 9 10 10 Mean (mm) Mean (mm) SD SD SE (mm) SE (mm) RE (%) RE (%) Pommery et al. BMC Ecol Evo (2021) 21:136 Page 7 of 19 Height 7_4 Height 7_8 Height 2.66 3.02 2.66 3.06 2.68 3.04 2.72 3.04 2.7 3,00 2.68 3.04 2.646 3.04 0.084 2.98 0.027 3,00 1.008 3,00 3.022 0.026 0.004 0.132 Width 7_4 Width 7_8 Width 9.6 9.26 9.68 9.12 9.62 9.04 9.7 9.06 9.6 9.06 9.56 9.08 9.65 9.1 0.069 9.06 0.022 9.08 0.228 9.04 9.09 0.065 0.02 0.225 0.03 0.01 0.059 0.022 0.007 0.052 Length 7_4 Length 7_8 Length 16.32 13.42 16.28 13.36 16.3 13.38 16.3 13.38 16.3 13.4 16.28 13.38 16.31 13.34 13.38 13.38 13.36 13.378 Height 7_3 Height 7_7 Height 2.78 3.04 2.86 3.18 2.84 3.04 2.84 2.98 2.76 3.02 2.82 3.02 2.8 3,00 0.043 3.04 0.014 3.06 0.488 3.04 3.042 0.054 0.017 0.558 Width 7_3 Width 7_7 Width 9.06 8.7 9.06 8.4 9.04 8.54 9.04 8.56 9.02 8.56 9.04 8.6 9.032 8.66 0.036 8.58 0.011 8.6 0.124 8.66 8.586 0.083 0.026 0.307 0.062 0.02 0.155 0.043 0.014 0.118 Length 7_3 Length 7_7 Length 12.64 11.5 12.66 11.38 12.64 11.5 12.64 11.5 12.62 11.5 12.64 11.52 12.624 11.5 11.54 11.52 11.5 11.496 Height 7_2 Height 7_6 Height 2.72 2.44 2.7 2.52 2.7 2.58 2.72 2.56 2.68 2.56 2.7 2.54 2.692 2.58 0.042 2.58 0.013 2.58 0.498 2.52 2.546 0.044 0.014 0.55 Width 7_2 Width 7_6 Width 9.08 8.02 9.1 7.92 9.06 7.92 9.14 7.94 9.08 7.94 9.06 8,00 9.062 8,00 0.048 7.92 0.015 7.96 0.169 7.92 7.954 0.039 0.012 0.155 0.109 0.034 0.298 0.043 0.014 0.088 Length 7_2 Length 7_6 Length 11.58 15.58 11.6 15.46 11.56 15.44 11.58 15.44 11.58 15.46 11.56 15.44 11.524 15.48 15.46 15.44 15.44 15.464 Height 7_1 Height 7_5 Height 2.96 2.66 2.98 2.96 2.92 2.96 2.96 2.92 2.98 2.92 2.9 2.92 2.926 2.94 0.045 2.94 0.014 2.94 0.489 2.94 2.91 0.089 0.028 0.968 Width 7_1 Width 7_5 Width 9.74 7.8 9.74 7.9 9.84 7.92 9.74 7.9 9.74 7.92 9.74 7.94 9.748 7.94 0.082 7.96 0.026 7.92 0.265 7.96 7.916 0.046 0.015 0.184 Length 7_1 Length 7_5 Length 15.88 14.22 15.9 13.8 15.92 14,00 15.92 14.28 15.9 14.1 15.88 13.94 15.918 14.08 0.07 14.04 0.022 14.08 0.138 14.04 14.058 0.134 0.043 0.303 (continued) 1 Table Measurement Measurement in millimetres. are values The 8.1. taken on Avizo were measurements The also added. (RE) were error (SE), and the relative error the standard (SD), deviation mean, the standard The 5 1 6 2 7 3 8 4 9 5 10 6 Mean (mm) 7 SD 8 SE (mm) 9 RE (%) 10 Mean (mm) SD SE (mm) RE (%) Pommery et al. BMC Ecol Evo (2021) 21:136 Page 8 of 19

Table 2 Means of the repeated measurements of the length, width, and height of each segmented replacement (repl.) and functional (fct.) tooth in the studied Henodus chelyops specimens, as well as the overall mean Specimen Length_repl Width_repl Height_repl Length_fct Width_fct Height_fct

III 11.4 7.34 2.5 9.85 5.7 2.41 III 12.31 7.33 2.26 10.32 6.7 2.33 III 12.93 7.6 2.36 10.58 6.28 2.59 III 13.32 7.74 2.22 12.19 6.72 2.66 VII 11.5 8.59 3.04 11.52 9.06 2.69 VII 12.62 9.03 2.8 13.38 9.09 3.02 VII 15.46 7.95 2.55 14.06 7.92 2.91 VII 16.31 9.65 2.65 15.92 9.75 2.93 Mean 13.231 8.154 2.547 12.227 7.652 2.692

with a p-value of 0.0294. It is not the case in speci- a lingual position to the functional tooth in Sauroptery- men GPIT-PV-30007, with a p-value of 0.6857. It is not gia [32, 33, 50]. Eosauropterygia, such as Nothosaurus, possible to conclude about a width difference between has a quite horizontal tooth replacement [32] (Fig. 6), the functional and the replacement teeth in H. chely- whereas the tooth replacement in Palatodonta bleekeri ops. The p-value of the length difference between the remains unknown [2]. We suggest that this species had replacement and functional teeth in specimen GPIT- a horizontal tooth replacement similar to Eosauroptery- PV-30003 is quite close to 0.05. Even if the p-value gia, because it also carries pointed teeth and that vertical is higher than 0.05, this threshold is quite subjective tooth replacement is linked to the subsequent fattening [47]. Thus, the possibility that lengths are significantly of the crushing teeth. equivalent should not be ruled out in particular with Cranial material of Paraplacodus is scarce and poorly regard to the low sample analyzed in this study. There preserved to study its tooth attachment and replacement is no confirmation of variation of tooth size either [32, 34]. Following Rieppel [32], in P. g igas, the position of between several specimens in H. chelyops nor between the replacement premaxillary teeth is posteroventral for functional and replacement teeth in a single individual. premaxillary teeth and posterodorsal for anterior den- The measurements of the anterior and posterior tary teeth. Tis hypothesis is supported by the presence teeth of different Cyamodontoidea from the stud- of small opened foramina behind the alveoli of the func- ies of Rieppel and Hagdorn [48], Rieppel [26], Miguel tional teeth. Chaves et al. [8], and Wang et al. [15] were transcribed As regards the fattened and enlarged crushing teeth in in Table 3 and plotted in Fig. 5. The mean tooth length placodonts, the replacement teeth cannot grow in a lin- and width of each tooth in H. chelyops from the pre- gual position to the functional teeth because of their tight sent study were also added to this diagram. The length spatial arrangement on the maxilla, the palatine, and the of the posterior palatine teeth in Cyamodontidae and posterior part of the dentary [32]. Tin sections exhibit a Placochelyidae is always longer than 25 mm and their vertical replacement in P. g igas, cyamodontids, and pla- width wider than 17 mm. In comparison, the palatine cochelyids [1, 2, 32, 33] (Fig. 6). A large replacement cav- teeth in H. chelyops have smaller dimensions. The ity is visible just below the functional tooth, separated by teeth of H. chelyops are approximatively half the length a narrow horizontal shelf (Fig. 2). A wide opening deep and one third of the width of the posterior-most teeth to the functional tooth exposes the replacement tooth of other Cyamodontoidea. However, the teeth of H. [32]. When the functional tooth falls out, the horizon- chelyops and the anterior palatine teeth of other Cya- tal shelf is resorbed by the replacement tooth before it modontoidea are similar in length. moves upwards into the functional position. Tis study shows that despite the reduced size of the crushing Discussion teeth, vertical tooth replacement is also visible in H. che- Tooth replacement in Placodontia lyops (Fig. 2). Vertical tooth replacement is a character Several studies provide discussion on tooth replace- shared by both non-cyamodontoid and cyamodontoid ment in Sauropterygia [1, 32, 33, 49, 50]. Generally, the placodonts and could be a potential apomorphy of pla- replacement tooth grows in distinct alveolar spaces, in codonts within Sauropterygia. In H. chelyops and other Pommery et al. BMC Ecol Evo (2021) 21:136 Page 9 of 19

Fig. 4 A Boxplots comparing the length (a), the width (b), and the height (c) between both specimens GPIT-PV-30003 and GPIT-PV-30007 of Henodus chelyops and between their replacement and functional teeth. The thick black lines represent the medians. The values are in millimeters. B Bivariate diagrams between the replacement and the functional tooth size in both H. chelyops specimens. The length diference (a) is illustrated at the top, the width diference (b) at the middle and the height diference (c) at the bottom. The values of the teeth of specimen GPIT-PV-30003 are represented by triangles and ones of specimen GPIT-PV-30007 are represented by squares. The values are in millimeters

placodonts, only one generation of tooth replacement tooth replacement strategy were selected to make up for a was observed. In both studied H. chelyops specimens, the potentially hasty failure of the functional tooth while nego- replacement teeth seem to have fully developed enamel. tiating spatial constraints [33]. Non-cyamodontoid placo- Te unique pattern of tooth replacement in placodonts donts experiencing high dental wear exhibit a relatively is the result of phylogenetic trends associated with their frequent tooth replacement [27–29, 33]. Indeed, their con- durophagous diet [33]. Te reduction of the crushing vex crushing teeth are more prone to dental failure under tooth number in advanced placodonts and a particular high loads. No discernable tooth replacement pattern was Pommery et al. BMC Ecol Evo (2021) 21:136 Page 10 of 19

Table 3 Length and width of the anterior and posterior palatine teeth of diferent taxa in Cyamodontoidea used in Fig. 5 Taxon Specimen Position Tooth_Length Tooth_Width

Cyamodus rostratus UMO BT 748 (holotype) Anterior 8.7 8.6 Posterior 27.5 23.2 Cyamodus muensteri BMNH R1644 Anterior 21.5 17.8 Posterior 44.3 33 Cyamodus kuhnschnyderi MHI 1294 Anterior 19.1 18.2 Posterior 44.2 37.7 Cyamodus orientalis ZMNH M8820 (holotype) Anterior 20 20 Posterior 40 40 Macroplanus raeticus BSP 1967 1 324 (holotype) Anterior 21.2 19.8 Posterior 68.5 48.5 Parahenodus atancensis MUPA ATZ0104 (holotype) Posterior 13 7 Placochelys placodonta FAFI Ob/2323/Vt.3 (holotype) Anterior 13.8 11 Posterior 27.2 20.8 Psephoderma alpinum MSNM V471 Anterior 7.5 6.4 Posterior 25.2 17 Protenodontosaurus italicus MFSN 1819GP (holotype) Anterior 12.8 13.3 Posterior 36 28.5

Data mainly sourced from Rieppel [26] supplemented with measurements of Cyamodus kuhnschnyderi from Rieppel and Hagdorn [48], Parahenodus atancensis from Miguel Chaves et al. [8], and Cyamodus orientalis from Wang et al. [15]. The values are in millimetres

Fig. 5 Bivariate diagrams of the tooth length and width in diferent Cyamodontoidea members. The red and green points, respectively, correspond to the teeth of specimens GPIT-PV-30003 and GPIT-PV-30007 from Henodus chelyops. The anterior palatine teeth of other Cyamodontoidea members are represented by black points and the posterior teeth by blue points. The values, in millimeters, are transcribed in Table 3 Pommery et al. BMC Ecol Evo (2021) 21:136 Page 11 of 19

Fig. 6 Diversity of the dentition, the tooth replacement, and the palatine tooth morphology inside the placodont phylogenetic tree. The ventral views of the diferent placodont skulls come from Crofts et al. [29] except for the Henodus chelyops skull that was modifed from Mazin [24], and the P. atancensis skull that was modifed from Miguel Chaves et al. [8]. The lingual and vertical tooth replacement representations were made by Rieppel [17]. The lingual tooth replacement is based on his observations on Nothosaurus (Eosauropterygia) and the vertical tooth replacement is based on Placodus gigas (Placodontia). The occlusal surface shapes were redrawn after Crofts [27, 28] and Crofts et al. [29]. The cladogram is based on the phylogenetic analysis from Wang et al. [16]

noticed in early emerging placodonts [33]. Te Placodus functional units [33]. Teeth are unilaterally replaced in maxillary and palatine teeth are almost simultaneously each unit to maintain the crushing function on one side of replaced in order to restrict the breaking down of the sepa- the mouth. In H. chelyops, all palatine and dentary replace- ration between juxtaposed replacement alveoli destabiliz- ment teeth seem to grow at the same time, because a ing the support of the functional teeth [32]. Rieppel [32] replacement tooth is situated below each functional tooth considered that the replacement tooth in placodonts is in both examined H. chelyops specimens. It is not possible bigger than the preceding functional tooth, especially in to conclude about the frequency of the tooth replacement juveniles. However, spatial constraints control the maxi- in H. chelyops with the little data currently available. mum size of each tooth generation. In general, it seems as if there were no distinct regularities of tooth replace- Placodont tooth morphology ment rates in Placodontia [32]. Crofts et al. [29] noticed Te highly reduced number of crushing teeth in H. che- the tooth replacement rates are weaker in placochelyids lyops sets it apart from other placodonts even if the more than in the non-cyamodontoid placodonts despite their advanced placodonts seem to have fewer crushing teeth low number of maxillary and palatine teeth. In cyamo- than the more ancestral ones (Table 4). Our study reports dontoids, the dentition is divided in specifc and efective small and oval crushing palatine teeth in H. chelyops Pommery et al. BMC Ecol Evo (2021) 21:136 Page 12 of 19

Fig. 7 A Examples of small and large prey item dental loading regimes according to occlusal surface models: concave (left), fat (middle), and cusped (right), redrawn after Crofts [27, 28]. Red bars and arrows represent the location and direction of applied load for the small (up) and large (down) loading regimes across a representative range of tooth model appearances. B Macroscopic picture of the imprint of an Estheria shell collected by Reif [59] (GPIT-PV-30799). Estheria is characteristic for the “Gipskeuper Formation” (equivalent to the Grabfeld Formation) in Tübingen/ Lustnau where the diferent Henodus chelyops specimens were found. 2D slice (C) and 3D representation (D) of a gastropod shell found in the matrix attached to the skull of the specimen GPIT-PV-30003 of H. chelyops. E 3D representation of the gastropod shell on the occlusal surface of the H. chelyops tooth. F Hypothetical reconstruction of the jaw adductor musculature in H. chelyops, redrawn and colorized after Rieppel [3]. The nervus trigeminus innervated muscle is represented in orange and the nervus facialis innervated muscle (m. depressor mandibulae) in green. G Reconstruction of the crushing function of the palatine (green) and dentary (blue) teeth in H. chelyops. The hypothetical well-developed 1b-portion of musculus adductor mandibulae externus superfcialis (orange) could facilitate lateral jaw movement in H. chelyops

confrming Reif’s and Stein’s research [31]. Te central length of the palatine teeth. Te mean length of palatine concavity of the occlusal surface, observed in this study, teeth in specimens GPIT-PV-30003 and GPIT-PV-30007 was not reported by the authors. Nevertheless, they are 11.61 and 13.85 mm, respectively. Specimen GPIT- noticed the crushing teeth have a fat crown with a mar- PV-30003 has a ratio of tooth length/tooth width of about ginal swelling as well as the presence of fne pits. Reif and 1.68 and specimen GPIT-PV-30007 of about 1.57 (Fig. 5). Stein [31] considered the height of the tooth crown to be Rieppel [26] also calculated the ratio of the tooth length 2 mm. For these authors, the palatine teeth in H. chely- divided by the tooth width in several species inside the ops are 16–18 mm long and 8 mm wide and the dentary genus Cyamodus fnding ratios ranging between 1.16 and teeth are 13–14 mm long and 7–9 mm wide. Tese values 1.41, with Cyamodus tarnowitzensis having the highest. are approximately the same in our study except for the Pommery et al. BMC Ecol Evo (2021) 21:136 Page 13 of 19

Table 4 Skull morphological description of diferent genera included within Placodontia Taxon Paraplacodus Placodus Cyamodus Placochelys Psephoderma Henodus

Premaxillary teeth Number & Shape 3 long, procum- 3 long, 1 to 2 reduced 0 0 0 bent and procumbent, and blunt pointed spatulated and widely spaced Maxillary teeth Number & Shape 7 max. low and 3–5 low and 2–3 hemispheri- 3 fattened 2 fattened 0 rounded with a rounded (« bul- cal (posterior one central cusp bous») with a is elliptical) central cusp Size Quite large Quite large Increasing rear- Increasing rear- Posterior one is - wards wards larger Palatine teeth Number & Shape 4 low (3 posterior 3 quadrangular 2–3 circular or 2 fattened with a 2 Flattened with 1 with a fat are rectangular) elliptical central cusp a central cusp crown and (posterior one is covered ovoid) by fne pits Size More large than Large Very big (poste- Very big (poste- Very big (poste- Quite small maxillary teeth rior one is the rior one is the rior one is the tallest) tallest) tallest) Rostrum Shape Wide Wide Narrow Narrow, edentu- Very thin and Rectangular lous long, edentu- and wide, lous denticles

The shape of the rostrum and the number, the shape and the size of teeth (premaxillary, maxillary, and palatine teeth) have been considered. The morphological descriptions come from v. Huene [18], Mazin [24], Reif and Stein [31], and Rieppel [26, 41]

Despite the fragmented skull of the unique specimen While the other placodonts have fattened or slightly (MUPA ATZ0104) attributed to P. atancensis, it is pos- convex palatine teeth, the occlusal surface of the pala- sible to analyze its right palatine crushing tooth [8, 38]. tine teeth in Placochelyidae, such as Placochelys or Pse- Te morphology of the palatine teeth in P. atancensis and phoderma, and in Henodontoidae is rather concave [29] H. chelyops is comparable. Te right palatine tooth in P. (Fig. 6). Te Cyamodus premaxillary and maxillary teeth atancensis is also ovoid. Miguel Chaves et al. [8] observed are more fattened than in Paraplacodus and Placodus. a complex dental morphology corresponding to a central Even if the caudal-most palatine teeth of some Cyamo- concavity with a lateral elevation or crest. Te unique dus specimens (SMNS 91472 and MB.R.1773) are slightly entire palatine tooth measures 13 mm in length and concave, Crofts et al. [29] considered them as function- 7 mm in width which is quite similar to H. chelyops teeth. ally fat. Placochelyidae has a distinguished complex pala- However, Miguel Chaves et al. [8] considered the palatine tine tooth morphology with a median cusp and crescent teeth in P. atancensis to be proportionally bigger than furrows [27–29] (Fig. 6). Finally, it is possible to establish the palatine teeth in H. chelyops comparing their length three diferent tooth morphotypes for the palatine teeth with the width on the articular condyle of the quadrate. within Placodontia. (A) Non-cyamodontoid and cyamo- Indeed, the length of the palatine teeth in P. atancensis dontid placodonts have palatine teeth with a convex or is close to the width of the articular condyle of the quad- fattened occlusal surface. (B) Henodontoidae, including rate, whereas it is less than half in H. chelyops. H. chelyops, have concave palatine teeth without a central Te palatine teeth have diferent appearances among cusp. (C) Placochelyidae have concave palatine teeth with placodont groups. In non-cyamodontoid placodonts, a central cusp. they are rather rectangular or quadrangular, whereas in Cyamodontoidea they have a circular, elliptical, or ovoid Feeding strategies and habitat in Placodontia shape [9, 24, 27–29, 33] (Fig. 6). It is worth noting that Generally, it is believed that placodonts fed on bivalves, Cyamodontoidea literally means “bean-shaped teeth”. brachiopods, and maybe decapod crustaceans [20, 37]. Te occlusal surface morphology is quite diferent among Tese hard-shelled invertebrates are often present in the the placodonts [27–29] (Fig. 6). Crofts et al. [29] studied same deposits as placodonts [20, 27, 51]. Tis specifc diet the evolution of the occlusal morphology and the “fat- brought placodonts to stay in shallow water in nearshore tening” of the teeth in diferent placodonts by measuring environments, which is suggested by the sedimentary their radius of curvature. facies where they were discovered [20, 24]. Non-cyamo- dontoid placodonts are only known in epicontinental Pommery et al. BMC Ecol Evo (2021) 21:136 Page 14 of 19

seas whereas Cyamodontoidea was present in both epi- [29]. It would be worth testing whether the occlusal continental seas and the Tethys [52]. surface morphology of palatine teeth in H. chelyops Henodus chelyops is known as inhabiting a brackish could prevent a hasty loosening or break of the tooth lagoon environment [21, 25, 41, 52, 53]. Te potential and indicate whether its dental morphology is adapted food resources are quite scarce in the Oberer Gipskeuper to small or large prey items. Te likelihood of failure deposits from Tübingen-Lustnau. Estheria-crustaceans and the pressure applied to break and to crush the prey and some fshes, molluscs, and gastropods are present items are not the same according to the tooth occlusal [31, 39, 52]. Te short and oval palatine teeth in H. che- morphology. Te concavity of the occlusal surface, such lyops, its extremely reduced tooth number, and the coro- as in H. chelyops palatine teeth, generates a pressure noid process morphology may raise the question of their diference when the invertebrate items are crushed [27, crushing efectiveness and resistance to hard-shelled 28] (Fig. 7A). If the shell item is small, the pressure is molluscs. Tat is why the majority of the researchers concentrated on the center of the concavity, whereas if do not consider H. chelyops as having had a strongly the shell item is large, the pressure is put on the mar- durophagous diet consisting of thick-shelled molluscan ginal border of the occlusal surface (Fig. 7A). For fat prey items like other placodonts certainly did [8, 20, 27, teeth, the load of the large prey items is spread over 31, 37, 41, 42, 54]. the entire occlusal surface if the prey item is fat [27, Te H. chelyops skull morphology indicates a low 28]. Tis model hardly ever happens, since the shells of degree of durophagy and bite force. Henodus chelyops has invertebrates are mostly rounded. On the contrary, the been interpreted as herbivorous, as a flter-feeder, or as loading regime of round hard-shelled items is concen- both [20]. Tis taxon has been considered herbivorous trated in the middle of the occlusal surface of fat teeth. because of its cutting edge on the premaxilla with the Tus, concave teeth require more force to break shells row of tooth-like denticles which could scrape the plants than fat teeth and convex teeth [27, 28, 58]. However, of the substratum [31, 42]. Reif and Stein [31] also con- greater strains were applied to convex teeth that means sidered the grooves with baleen-like structures as a flter there is a greater likelihood of crack formation in con- or allowing the ejection of superfuous water. Herbivo- vex teeth than in concave or fat teeth for large or small rous marine reptiles are still unusual [42]. Filter-feeding prey items [27, 28]. has also been proposed in H. chelyops by other authors According to the patterns of strain set up by Crofts [8, 18, 27, 41, 55]. Te spatulate rostrum would have cut et al. [27, 28], the concave teeth can undergo ring cracks the aquatic vegetation before being fltered out [8]. Te and edge failures if the strains are too high. Tis would rostrum of H. chelyops was compared to the spatulate be a reason why concave tooth appearances are not as rostrum of Atopodentatus unicus, which was interpreted common as convex tooth appearances in nature [27, 28]. as flter feeder and herbivorous [56, 57]. H. chelyops was However, the morphology of concave teeth implies the also declared as a suction feeder due to its massive hyoid applied load is distributed over the entire occlusal sur- apparatus [54]. Te extreme tooth reduction of this spe- face reducing dental wear. Ten, the tooth is functional cies is a relevant argument to explain a fltering diet in over a longer period, because the enamel stays thick this species. enough to prevent subsurface cracks caused by strains Te crushing dentition of placodonts represents one of the invertebrate items. It is also possible to reduce the of the most extreme forms of durophagy that has ever applied stress on concave teeth if the item has a whorl as existed [33]. Durophagy corresponds to the diet of seen in gastropods. Te concave tooth morphology, such hard-shelled organisms like molluscs or crustaceans. as in H. chelyops, increases the area the tooth is in con- Durophagous animals needed high bite forces [27, 28]. tact with the small items [27, 28]. H. chelyops could crush Teir feeding habit is associated with diferent mor- more easily the shelled prey items in the depression of phological adaptations, such as a change of the teeth the occlusal surface. Te longitudinal crest present in the position, a robust or heavy skull architecture, or a large occlusal surface of the crushing teeth in placochelyids temporal skull region for jaw muscle attachments that also covers more surface of the shell items than convex are found in the more deeply nested placodonts. Te or fat teeth and could ofset a lack of bite forces in these crushing teeth of durophagous predators, such as pla- derived placodonts. In at least some cyamodontids, the codonts, have evolved to resist failure against hard- repartition of the efective force applied to a shell across shelled prey [28]. Tis illustrates how the evolutionary the dentition could be balanced. pressure between the prey and the predators can have Multiple small gastropod shells were found within the an infuence on the dental morphology. Te diferences attached matrix in both H. chelyops specimens (Fig. 7C– in tooth occlusal morphology indicate that placodonts E). One of these is present close to the right functional have evolved diferent durophagous specializations dentary tooth and a second specimen was encountered Pommery et al. BMC Ecol Evo (2021) 21:136 Page 15 of 19

between the right quadrate and the articular of the speci- extreme tooth reduction and the small size of its crushing men GPIT-PV-30003. Te taxonomic identifcation of teeth imply that the durophagy is moderate only in heno- these gastropods was not achieved in this study. Tese dontid species. Te concavity of the occlusal surface in gastropod shells measure around 3 mm in length. Tis H. chelyops appears more adapted to crushing small prey invertebrate looks like a potential candidate as a food items. Tis concavity could also be an advantage against source for H. chelyops even if these small invertebrates the failure likelihood in contrast to convex teeth. It would seem to be not very proftable in terms of energy cost be important to understand if the diferent tooth mor- and beneft. Te small crustacean Estheria, which is quite photypes within Placodontia are the results of changes in frequent in the deposits from the Grabfeld Formation feeding behavior or correspond to diferent feeding strat- (formerly “Gipskeuper Formation”) in Germany, could egies in order to be more efcient to crush hard-shelled also be preyed upon by H. chelyops [59] (Fig. 7B). Tese prey. Te tooth replacement in H. chelyops is vertical as hypotheses are admissible only if the deposit environ- observed in Placodus gigas and Cyamodontoidea. Tis ment where the H. chelyops remains were found corre- study reinforces the hypothesis of generalized vertical sponds to its habitat. Tis has not yet been fully verifed tooth replacement across Placodontia. It seems highly [60]. We propose that H. chelyops had a multifaceted diet. improbably that the vertical tooth replacement indepen- Tanks to its specifc dentition, H. chelyops could crush dently arose in each group. Tis study has the particular with its palatine teeth invertebrates such as gastropods perspective of helping to perceive the most reliable func- that are feeding on aquatic vegetation while cropping tion of the dentition of H. chelyops (cutting edges, baleen- them with its fat rostrum. Tese invertebrates could pro- like structures, and crushing palatine and dentary teeth). vide supplementary proteins in addition to the aquatic plants and potentially plankton from flter feeding. Materials & Methods Te motion of both jaws to crush the invertebrate items Specimens and tomographic scans with the concave teeth in H. chelyops could actually be v. Huene [18, 64–66], Reif [53], and Fischer [60] quite particular. Rieppel [3] studied the jaw musculature described the eight H. chelyops individuals uncov- of H. chelyops based on its wide skull and the specifc ered thus far, which are all stored in the Paleonto- anatomy of the temporal skull region (Fig. 7F) and con- logical Collection of the University of Tübingen. All cluded that the H. chelyops skull does not indicate high individuals preserve the skull, except for specimen VIII bite forces. Te hemimandibles are not strongly fused at (GPIT-PV-30008; Roman numerals, as conventional in their symphysis and the articulation between lower jaw Henodus-literature, designate their original succession of and quadrate is relatively complex [26, 34, 61] possibly excavation). Te well-preserved skulls of specimens III enabling more intricate movements than just opening (GPIT-PV-30003) and VII (GPIT-PV-30007) were sub- and closing of the jaw. A hypothetical 1b-portion of mus- jected to synchrotron visualization to be analyzed in this culus adductor mandibulae externus superfcialis, con- study. necting the quadratojugal with the lateral surface of the Specimen GPIT-PV-30003, previously freed from the lower jaw, however, could be well-developed [41] (Fig. 7F matrix by preparator Wilhelm Wetzel, was described and G). With that, an asymmetrical positioning of small by v. Huene [54]. Te carapace and pelvic girdle of this prey items in the embayment of the crushing teeth on specimen are preserved but the caudal vertebrae are lack- the left or the right side of the mouth (sensu Druzinsky ing. Although several cracks have propagated the skull & Greaves 1979 [62]) and even some lateral movement of specimen GPIT-PV-30003, it represents the best-pre- might have been possible. In this context, the tips of the served H. chelyops skull available today. Measuring 16 cm more fragile edges of the concave teeth [27, 28] would in length and 10.5 cm in width, the skull of specimen likely not directly contact each other and prevent break- GPIT-PV-30003 is slightly compressed on its anterior age—similar to the molars of mammals [63] (Fig. 7G). part and the mandible remained in full articulation with the cranium. Conclusions Specimen GPIT-PV-30007, which features a reasonably New synchrotron CT-scans of the skull of two H. chely- well-preserved carapace, has not been reported in sci- ops specimens provide novel insights into the diversity of entifc literature. Its skull has not been prepared before dental morphology and replacement in placodonts. Mor- tomographic visualization but its dorsal surface is visible phological analysis of the occlusal surfaces of H. chely- in external view and appears to accommodate upper tem- ops teeth revealed that this species carries concave teeth poral fenestrae. Te skull of specimen GPIT-PV-30007 without a central cusp, which are otherwise reported measures 16 cm in length and maintains the original only for Parahenodus atancensis. Tis confrms variable articulation between cranium and mandible. degrees of durophagy within Placodontia. Indeed, its Pommery et al. BMC Ecol Evo (2021) 21:136 Page 16 of 19

Both specimens were characterized using propaga- fnally exported as a stack of non-compressed tif images. tion phase contrast synchrotron X-ray micro com- To facilitate data handling, a binning 2 × 2 × 2 was gen- puted tomography (PPC SRµCT) at the ID17 beamline erated during the post processing, reducing the data size of the European Synchrotron Radiation Facility (ESRF, by 8, generating datasets with an isotropic voxel size of Grenoble France). Te X-ray setup consisted of: X-ray 93.84 µm. beam from a wiggler (W150D, gap 26 mm) and a Si 111 double-bent Laue monochromator (set at 120 keV for Morphology and size measurements specimen GPIT-PV-30003 and 132 keV for specimen We analyzed the functional morphology and replacement GPIT-PV-30007). Images were recorded with an indirect mode of the crushing teeth in both H. chelyops speci- detector comprising a 2 mm thick Yttrium Aluminum mens. Te conditions are described and statistically com- Garnet (YAG) scintillator, × 0.25 magnifcation from a pared to each other and to other placodonts. Te stack set of optical lenses and a FReLoN 2 k charge-coupled of tomograms (i.e., slices from the computed tomogra- device (CCD) camera (using the frame transfer and pre- phy reconstruction) was imported in Avizo 8.1 software cision modes). Te pixel size for the recorded images of [71] to segment the teeth and generate 3D rendering. Te 46.92 µm was obtained measuring the shift of a metal- functional and replacement teeth of both skulls were vir- lic rod moved using a translation motor perpendicular tually extracted using manual segmentation in Avizo 8.1 to the X-ray beam. Given the energy and pixel size, the (e.g., Fig. 2). Te external surfaces of the skull and of each specimens were placed 11 m in front of the detector to segmented tooth were converted into a mesh and saved maximise contribution of phase contrast efect. Te beam as “PLY” fles. Tese elements were projected as 3D mod- size varied on the vertical axis depending on the energy els in the freeware solution MorphoDig 1.5 [72]. Inside used: 7.98 × 46.43 mm (vertical x horizontal) for the their respective skull rendered at 80 percent transpar- 120 keV setup and 7.04 × 46.43 mm (v × h) for 132 keV. ency, each individual tooth was projected opaque to visu- Slightly diferent protocols were used for each specimen. alize its position and placement. All replacement and functional teeth of both H. chely- • Specimen GPIT-PV-30007: acquisition of this speci- ops specimens were measured. We assessed whether the men was more classic (no attenuation or half acqui- replacement teeth were larger than the functional teeth, sition protocol), necessitating 43 acquisitions on the which is what Rieppel [32] suggested for—especially vertical axis, moving the sample by 3.8 mm between juvenile—Placodus gigas and could imply a gradual each acquisition. Each acquisition consisted of 4998 increase of placodont tooth size during ontogeny. Anter- projections of 0.15 s exposure each. oposterior length, mediolateral width, and dorsoventral • Specimen GPIT-PV-30003: as the specimen was height of each tooth was determined using the 2D Length larger than the feld of view, we used the so-called Tool in Avizo 8.1. Representative locations for the half-acquisition protocol, where the rotation axis of referred dimensions were identifed through 3D render- the sample stage is shifted (here shifted by 38.44 mm) ings of the teeth in occlusal (length and width) and lin- to the side of the recorded images [67]. We also used gual view (height; see Fig. 3). Each measurement was the attenuation protocol, to compensate for the high conducted ten times to allow for assessment of the meas- X-ray attenuation of the specimen [67], plunging the urement error of manual segmentation in both speci- specimen in a 16 cm diameter tube flled with 5 mm mens. Furthermore, each set of three complementary diameter aluminum balls. Tomographic acquisitions measurements was obtained from de novo oriented teeth consisted of 4998 projections of 1 s exposure each, to mitigate bias in standard orientation. Te standard over a 360° of the sample. Tirty-two acquisitions error (SE) was calculated by dividing the standard devia- were necessary to compensate for the limited verti- tion (σ) over the square root of the number of repeated SE σ cal size of the beam, moving the sample by 5.8 mm independent measurements (N): = √N . Relative error between each acquisition. (RE) was quantifed as a percentage of the measured val-

ues by dividing the standard error overSE the mean of the Te computed tomography reconstruction was per- RE repeated measurements (µ): = µ . Te mean of the formed with the software PyHST2 [68] using the single repeated measurements of tooth length, width, and distance phase retrieval approach [69]. After the com- height are here considered as the authentic values. puted tomography reconstruction, post processing of the Skull lengths were measured using the 2D Length data included: merging of the dataset along the vertical Tool in Avizo. Dental length, width, and height dimen- axis using a weighted average; correction of ring arte- sions of both specimens were plotted in bivariate fact on slices [70]; 32-bit to 16-bit conversion based on diagrams capturing the mean values of replacement 0.002% saturation of the 3D histogram, the data being teeth on the X-axis and the mean values of functional Pommery et al. BMC Ecol Evo (2021) 21:136 Page 17 of 19

teeth on the Y-axis. Tese diagrams show whether Declarations the diferent crushing teeth in a single specimen have Ethics approval and consent to participate a homogeneous size. Since the skulls of specimens Not applicable. GPIT-PV-30003 and GPIT-PV-30007 have very simi- Competing interests lar lengths (158.84 and 158.92 mm, respectively), The authors declare that they have no competing interests. we could establish whether both H. chelyops speci- mens exhibit dental size diferences independent from Author details 1 Senckenberg Centre for Human Evolution and Palaeoenvironment (HEP) growth bias. Boxplots showing the distribution of the an der Eberhard-Karls-Universität Tübingen, Sigwartstraße 10, 72076 Tübingen, functional and replacement tooth length, width, and Germany. 2 Fachbereich Geowissenschaften, Eberhard-Karls-Universität Tübin- height across the two specimens are also provided. Te gen, Hölderlinstraße 12, 72074 Tübingen, Germany. 3 Université de Bourgogne- Franche-Comté, Esplanade Erasme, 21000 Dijon, France. 4 Universität Zürich, tooth length, width, and height were also normalized by Paläontologisches Institut und Museum, Karl Schmid‑Strasse 4, 8006 Zürich, dividing them by the skull length. Indeed, the older a Switzerland. 5 Oxford University Museum of Natural History, University placodont is, the larger is the size of its crushing teeth of Oxford, Oxford, UK. 6 European Synchrotron Radiation Facility, 71 Avenue des Martyrs, 38000 Grenoble, France. 7 The Natural History Museum, Cromwell might be [32]. Ten, the links between length, width, Road, London SW7 5BD, UK. 8 Department of Organismal Biology, Uppsala and height of the replacement and functional teeth in University, Norbyvägen 18 A, 752 36 Uppsala, Sweden. 9 Naturalis Biodiver- H. chelyops were tested with the independent 2-group sity Center, Darwinweg 2, 2333 CR Leiden, the Netherlands. 10 Forschungs- Neutronenquelle Heinz Maier-Leibnitz, Lichtenbergstr. 1, 85748 Garching, Mann–Whitney U test on R Studio [73, 74]. To have Germany. no infuence from individuals, this test was carried out independently for both specimens. Finally, the tooth Received: 22 February 2021 Accepted: 17 May 2021 length and width in H. chelyops was plotted together with measures of other members of Cyamodontoidea in a bivariate diagram with the length on the X-axis and References the width on the Y-axis. 1. Neenan JM, Li C, Rieppel O, Scheyer TM. The cranial anatomy of Chinese placodonts and the phylogeny of Placodontia (Diapsida: Sauropterygia). 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